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Licensed Unlicensed Requires Authentication Published by De Gruyter July 27, 2019

Acoustic identification of two morphologically similar bat species, Miniopterus magnater and Miniopterus fuliginosus (Chiroptera, Miniopteridae)

Hui Wu, Tinglei Jiang, Sen Liu, Guanjun Lu and Jiang Feng
From the journal Mammalia

Abstract

Bats play important roles in ecosystems, and are thus considered bioindicators. Libraries of echolocation calls provide huge potential resources for bat species identifications, ecological studies and conservation surveys. Here, the echolocation calls of two morphologically similar bat species (Miniopterus magnater and Miniopterus fuliginosus) were recorded and described in order to characterize vocal signatures for field identification in China. Both M. magnater and M. fuliginosus emitted short frequency modulated echolocation calls with narrow bandwidths. Each call of the former species included two harmonics, with the first harmonic being the strongest, whereas calls of the latter species normally contained one harmonic. Although call durations were similar between the two species, there were significant differences in start, end and peak frequencies between M. magnater and M. fuliginous. The results showed that 92.3% of all calls recorded in China were attributed to the correct species based on spectral features of echolocation calls. We concluded that echolocation calls are valuable characters for the identification of morphologically similar bat species.

Funding source: National Natural Science Foundation of China

Award Identifier / Grant number: 31700331

Award Identifier / Grant number: 31872680

Award Identifier / Grant number: 31670390

Award Identifier / Grant number: 31870354

Award Identifier / Grant number: 31500307

Funding source: Fund of the Jilin Province Science and Technology Development Project

Award Identifier / Grant number: 20180101024JC

Funding statement: This research was supported by the National Natural Science Foundation of China (grant nos. 31700331, 31872680, 31670390, 31870354 and 31500307) and the Fund of the Jilin Province Science and Technology Development Project (grant no. 20180101024JC).

References

Ahlen, I. and H.J. Baagoøe. 1999. Use of ultrasound detectors for bat studies in Europe: experiences from field identification, surveys, and monitoring. Acta Chiropterol. 1: 137–150.Search in Google Scholar

Arias-Aguilar, A., F. Hintze, L.M.S. Aguiar, V. Rufray, E. Bernard and M.J. Ramos Pereira. 2018. Who’s calling? Acoustic identification of Brazilian bats. Mammal. Res. 63: 231–253.10.1007/s13364-018-0367-zSearch in Google Scholar

Barclay, R.M. 1999. Bats are not birds – a cautionary note on using echolocation calls to identify bats: a comment. J. Mammal. 80: 290–296.10.2307/1383229Search in Google Scholar

Barratt, E.M., R. Deaville, T.M. Burland, M.W. Bruford, G. Jones, P.A. Racey and R.K. Wayne. 1997. DNA answers the call of pipistrelle bat species. Nature 387: 138–139.10.1038/387138b0Search in Google Scholar

Bradbuty, J.W. and S.L. Vehrencamp. 2011. Principles of animal communication. Second edition. Sinauer Associates, Sunderland. pp. 750.Search in Google Scholar

Fenton, M.B. and G.P. Bell. 1981. Recognition of species of insectivorous bats by their echolocation calls. J. Mammal. 62: 233–243.10.2307/1380701Search in Google Scholar

Field, A. 2005. Discovering statistics using SPSS. Second edition. ISM introducing statistical methods. Sage, London. pp. 816.Search in Google Scholar

Fukui, D., N. Agetsuma and D.A. Hill. 2004. Acoustic identification of eight species of bat (Mammalia: Chiroptera) inhabiting forests of Southern Hokkaido, Japan: potential for conservation monitoring. Zool. Sci. 21: 947–955.10.2108/zsj.21.947Search in Google Scholar

Grant, B.R. and P.R. Grant. 1996. Cultural inheritance of song and its role in the evolution of Darwin’s finches. Evolution 50: 2471–2487.10.1111/j.1558-5646.1996.tb03633.xSearch in Google Scholar

Griffin, D.R. 1958. Listening in the dark. Yale University Press, New Haven. pp. 415.Search in Google Scholar

Jacobs, D.S. 1999. Intraspecific variation in wingspan and echolocation call flexibility might explain the use of different habitats by the insectivorous bat, Miniopterus schreibersii (Vespertilionidae: Miniopterinae). Acta Chiropterol. 1: 93–103.Search in Google Scholar

Jiang, Z.G. 2015. China’s mammal diversity and geographic distribution. Beijing Science Press, Beijing. pp. 416.Search in Google Scholar

Jones, G. 1997 Acoustic signals and speciation: the roles of natural and sexual selection in the evolution of cryptic species. Adv. Stud. Behav. 26: 317–354.10.1016/S0065-3454(08)60383-6Search in Google Scholar

Jones, G. and K.E. Barlow. 2004. Cryptic species of echolocating bats. In: (J. Thomas, C. Moss and M. Vater, eds.) Echolocation in bats and dolphins. Chicago University Press, Chicago, IL, USA. pp. 345–349.Search in Google Scholar

Jones, G. and B. Siemers. 2010. The communicative potential of bat echolocation pulses. J. Comp. Physiol. A 197: 447–457.10.1007/s00359-010-0565-xSearch in Google Scholar PubMed

Lawrence, B.D. and J.A. Simmons. 1982. Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. J. Acoust. Soc. Am. 71: 585–590.10.1121/1.387529Search in Google Scholar PubMed

Li, S., K. Sun, G. Lu, A. Lin, T. Jiang, L. Jin, J.R. Hoyt and J. Feng. 2015. Mitochondrial genetic differentiation and morphological difference of Miniopterus fuliginosus and Miniopterus magnater in China and Vietnam. Ecol. Evol. 5: 1214–1223.10.1002/ece3.1428Search in Google Scholar PubMed PubMed Central

Macías, S., E.C. Mora and A. García. 2006. Acoustic identification of mormoopid bats: a survey during the evening exodus. J. Mammal. 87: 324–330.10.1644/05-MAMM-A-124R1.1Search in Google Scholar

Papadatou, E., R.K. Butlin and J.D. Altringham. 2008. Identification of bat species in Greece from their echolocation calls. Acta Chiropterol. 10: 127–143.10.3161/150811008X331153Search in Google Scholar

Parsons, S. and G. Jones. 2000. Acoustic identification of twelve species of echolocating bat by discriminant function analysis and artificial neural networks. J. Exp. Biol. 203: 2641–2656.10.1242/jeb.203.17.2641Search in Google Scholar

Quinn, G.P. and M.J. Keough. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge. pp. 562.Search in Google Scholar

Robinson, M.F. 1996. A relationship between echolocation calls and noseleaf widths in bats of the genera Rhinolophus and Hipposideros. J. Zool. 239: 389–393.10.1111/j.1469-7998.1996.tb05459.xSearch in Google Scholar

Rodríguez-San Pedro, A. and J.A. Simonetti. 2013. Acoustic identification of four species of bats (Order Chiroptera) in central Chile. Bioacoustics 22: 165–172.10.1080/09524622.2013.763384Search in Google Scholar

Russo, D. and G. Jones. 2002. Identification of twenty-two bat species (Mammalia: Chiroptera) from Italy by analysis of time-expanded recordings of echolocation calls. J. Zool. 258: 91–103.10.1017/S0952836902001231Search in Google Scholar

Russo, D. and E. Papadatou. 2014. Acoustic identification of free-flying Schreiber’s bat Miniopterus schreibersii by social calls. Hystrix 25:119–120.Search in Google Scholar

Russo, D., M. Mucedda, M. Bello, S. Biscardi, E. Pidinchedda and G. Jones. 2007. Divergent echolocation call frequencies in insular rhinolophids (Chiroptera): a case of character displacement? J. Biogeogr. 34: 2129–2138.10.1111/j.1365-2699.2007.01762.xSearch in Google Scholar

Russo, D., L. Ancillotto and G. Jones. 2017. Bats are still not birds in the digital era: echolocation call variation and why it matters for bat species identification. Can. J. Zool. 96: 63–78.10.1139/cjz-2017-0089Search in Google Scholar

Rydell, J., H.T. Arita, M. Santos and J. Granados. 2002. Acoustic identification of insectivorous bats (order Chiroptera) of Yucatan, Mexico. J. Zool. 257: 27–36.10.1017/S0952836902000626Search in Google Scholar

Schnitzler, H.-U. and E. Kalko. 2001. Echolocation by insect-eating bats. Bioscience 51: 557–569.10.1641/0006-3568(2001)051[0557:EBIEB]2.0.CO;2Search in Google Scholar

Schoeman, M.C., S.M. Goodman, B. Ramasindrazana and D. Koubínová. 2015. Species interactions during diversification and community assembly in Malagasy Miniopterus bats. Evol. Ecol. 9: 17–47.10.1007/s10682-014-9745-4Search in Google Scholar

Seddon, N., C.A. Botero, J.A. Tobias, P.O. Dunn, H.E. MacGregor, D.R. Rubenstein, J.A.C. Uy, J.T. Weir, L.A. Whittingham and R.J. Safran. 2013. Sexual selection accelerates signal evolution during speciation in birds. Proc. R. Soc. B 280: 20131065.10.1098/rspb.2013.1065Search in Google Scholar PubMed PubMed Central

Shaw, K.L., C.K. Elliso, K.P. Oh and C. Wiley. 2011. Pleiotropy, “sexy” traits, and speciation. Behav. Ecol. 22: 1154–1155.10.1093/beheco/arr136Search in Google Scholar

Shi, L. M., J. Feng, Y. Liu, G.X. Ye and X. Zhu. 2009. Is food resource partitioning responsible for deviation of echolocation call frequencies from allometry in Rhinolophus macrotis? Acta Theriol. 54: 371–382.10.4098/j.at.0001-7051.099.2008Search in Google Scholar

Slabbekoorn, H. 2004. Singing in the wild: the ecology of birdsong. In: (P.R. Marler and H. Slabbekoorn, eds.) Nature’s music: the science of birdsong. Academic Press, Pittsburgh. pp. 178–205.10.1016/B978-012473070-0/50009-8Search in Google Scholar

Smith, A. and Y. Xie. 2008. A guide to the mammals of China. Princeton University Press, Princeton, 544 pp.Search in Google Scholar

Soisook, P., S. Bumrungsri, C. Satasook, V.D. Thong, S.S.H. Bu, D.L. Harrison and P.J.J. Bates. 2008. A taxonomic review of Rhinolophus stheno and R. malayanus (Chiroptera: Rhinolophidae) from continental Southeast Asia: an evaluation of echolocation call frequency in discriminating between cryptic species. Acta Chiropterol. 10: 221–242.10.3161/150811008X414818Search in Google Scholar

Sun, C., T. Jiang, J.S. Kanwal, X. Guo, B. Luo, A. Lin, and J. Feng. 2018. Great Himalayan leaf-nosed bats modify vocalizations to communicate threat escalation during agonistic interactions. Behav. Proc. 157: 180–187.10.1016/j.beproc.2018.09.013Search in Google Scholar PubMed

Thoisy, B.D., A.C. Pavan, M. Delaval, A. Lavergne, T. Luglia, K. Pineau, M. Ruedi, V. Rufray and F. Catzeflis. 2014. Cryptic diversity in common mustached bats Pteronotus cf. parnellii (Mormoopidae) in French Guiana and Brazilian Amapa. Acta Chiropterol. 16: 1–13.10.3161/150811014X683228Search in Google Scholar

Thong, V.D., S.J. Puechmaille, A. Denzinger, P.J.J. Bates, C. Dietz, G. Csorba, P. Soisook, E.C. Teeling, S. Matsumura, N. Furey and H.U. Schnitzler. 2012. Systematics of the Hipposideros turpis complex and a description of a new subspecies from Vietnam. Mammal Rev. 42: 166–192.10.1111/j.1365-2907.2011.00202.xSearch in Google Scholar

Tian, L., B. Liang, K. Maeda, W. Metzner and S. Zhang. 2004. Molecular studies on the classification of Miniopterus schreibersii (Chiroptera: Vespertilionidae) inferred from mitochondrial cytochrome b sequences. Folia Zool. 53: 303–311.Search in Google Scholar

Voigt, C.C. and T. Kingston. 2016. Bats in the anthropocene: conservation of bats in a changing world. Springer-Verlag, Berlin. pp. 606.10.1007/978-3-319-25220-9Search in Google Scholar

Walters, C.L., R. Freeman, A. Collen, C. Dietz, B.M. Fenton, G. Jones, M.K. Obrist, S.J. Puechmaille, T. Sattler, B.M. Siemers, S. Parsons and K.E. Jones. 2012. A continental-scale tool for acoustic identification of European bats. J. Appl. Ecol. 49: 1064–1074.10.1111/j.1365-2664.2012.02182.xSearch in Google Scholar

Wordley, C.F.R., E.K. Foui, D. Mudappa, M. Sankaran and J.D. Altringham. 2014. Acoustic identification of bats in the Southern Western Ghats, India. Acta Chiropterol. 16: 213–222.10.3161/150811014X683408Search in Google Scholar

Zamora-Gutierrez, V., C. Lopez-Gonzalez, M.C. MacSwiney, B.M. Fenton, G. Jones, E.K.V. Kalko, S.J. Puechmaille, V. Stathopoulos and K.E. Jones. 2016. Acoustic identification of Mexican bats based on taxonomic and ecological constraints on call design. Meth. Ecol. Evol. 7: 1082–1091.10.1111/2041-210X.12556Search in Google Scholar

Zhang, C., T. Jiang, G. Lu, A. Lin, K. Sun, S. Liu and J. Feng. 2018. Geographical variation in the echolocation calls of bent-winged bats, Miniopterus fuliginosus. Zoology 131: 36–44.10.1016/j.zool.2018.05.005Search in Google Scholar PubMed

Received: 2018-11-29
Accepted: 2019-07-03
Published Online: 2019-07-27
Published in Print: 2020-03-26

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